View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by UCL Discovery INSIGHTS | PERSPECTIVES SCIENCE GALLEY 1 2 3 4 PALEONTOLOGY 5 6 Artist impression goes here 7 Four legs too 8 9 10 many? 11 12 A long-bodied fossil snake re- 13 14 tains fore- and hindlimbs 15 By Susan Evans 16 A classic Gary Larson cartoon shows a 17 robed and bearded figure rolling out clay 18 strips, with the caption: “God makes the 19 snake.” Body elongation was certainly fun- 20 damental in the evolution of snakes from 21 lizards, as was the shrinking and ultimate- 22 ly the loss of limb pairs (limb reduction). 23 However, informative early fossils are rare, 24 and many details of the transition remain 25 unresolved. A remarkable fossil described 26 on p. xxx of this issue by Martill et al. (1) 27 brings fresh perspective to the debate. The 28 aptly named Tetrapodophis combines a 29 snakelike body with fore- and hindlimbs 30 bearing five well-developed digits. 31 Snakelike bodies evolved several times 32 through geological history. Among am- 33 niotes (reptiles, birds, and mammals), they 34 occur only in Squamata, the group com- 35 prising lizards and snakes. Within Squama- 36 ta, however, this body form has arisen in- 37 dependently at least 26 times (2) (see the 38 figure). Body elongation is always correlat- 39 ed with limb reduction (2), and the fore- 40 limbs are usually lost first (Bipes and Bach- 41 ia are rare exceptions). One explanation is 42 that as the body lengthens, coordination of 43 limb movements becomes increasingly dif- 44 ficult. Moreover, a serpentine body moves 45 most effectively by lateral undulation, a 46 movement in which limbs can become a 47 hindrance, especially in narrow spaces. Re- 48 searchers have identified a threshold body 49 length at which limb reduction begins, and 50 no known squamate with more than 70 51 precaudal (before tail) vertebrae retains 52 four complete limbs (2). Tetrapodophis (1), 53 54 Department of Cell and Developmental Biology, 55 University College London, London UK. 56 E-mail: [email protected] 57 58 59 sciencemag.org SCIENCE VOL. 349 • galley printed 6 July, 2015 • • For Issue Date: 24 July 2015 1 with around 160 precaudals, is therefore 1 Figure goes here 2 exceptional. 3 Efforts to reconstruct the evolutionary 4 stages in the snake body plan are ham- 5 pered by a lack of consensus on snake rela- 6 tionships and ancestral lifestyle. Analyses 7 using molecular data group snakes with 8 terrestrial lizards like iguanas and Komodo 9 Dragons (Iguania and Anguimorpha) (3) 10 and generally assume a burrowing or semi- 11 burrowing ancestry (1−3). However, some 12 analyses that include anatomical charac- 13 ters place them with extinct Cretaceous 14 (~100 to 66 million years ago) marine liz- 15 ards, the mosasaurs (3, 4). This has 16 prompted the suggestion of a marine 17 swimming ancestry for snakes (4). 18 Molecular divergence estimates date 19 snake origins to the Jurassic (~150 million 20 years ago) (5), but the earliest uncontested 21 fossils are isolated vertebrae from the mid- 22 Cretaceous (~113 million years ago) of 23 North America (5). These vertebrae come 24 from terrestrial deposits but are otherwise 25 fairly uninformative. More instructive are 26 several articulated skeletons or partial 27 skeletons from slightly younger (~100 mil- mental biology helps to explain how these regionalized pattern, implying that snakes 28 lion-year-old) deposits. The largest set con- changes occurred. Evolution of the snake have a neck of 10 to 12 segments. 29 sists of several related marine snakes from body form combined axial elongation, limb Like that of a lizard, the vertebral col- 30 the Middle East, North Africa, and south- loss, and reduced regionalization (8, 9). umn of Tetrapodophis has distinct regions, 31 ern Europe. These fossil snakes have 140 to Whether and how these components are including 10 to 11 short-ribbed neck verte- 32 155 precaudal vertebrae and a short tail. linked developmentally remains uncertain. brae adjacent to the tiny forelimbs. This 33 They show no trace of forelimbs or shoul- In all vertebrate embryos, individual verte- neck length is within the range of some 34 der girdle but do have small hindlimbs; on- brae develop from segments (somites) that generalized terrestrial lizards and matches 35 ly one [Haasiophis (6)] preserves digits. form at regular intervals. To increase ver- that proposed by the developmental (9, 11) 36 The relationships of these limbed marine tebral numbers, somite formation must ei- and anatomical (12) studies. Thus, as in 37 snakes remain controversial, but many ther continue for longer or occur at a faster long-bodied lizards, elongation of the snake 38 analyses (1, 3, 6, 7) nest them among mod- rate. Snakes use both strategies (8). Indi- skeleton occurred in the trunk region and 39 ern snakes, rather than nearer the base of vidual vertebrae then acquire positional not the neck. Moreover, if Tetrapodophis is 40 the snake evolutionary tree. This implies identity along the body axis through the correctly interpreted as a stem-snake, that 41 either that hind limbs were reduced more overlapping expression domains of Hox elongation preceded loss of the forelimbs. 42 than once within snakes, or that the limbs genes. In a typical tetrapod, the boundaries Love them or loathe them, snakes have 43 redeveloped in some lineages (6). between major vertebral regions (such as long fascinated humans. The combined ef- 44 A second set of early fossil snakes the neck and the trunk) coincide with Hox forts of paleontology and developmental 45 comes from terrestrial deposits in South gene expression boundaries. biology have gone some way toward un- 46 America. The most complete, 90-million- In a pioneering study of Python devel- ravelling the early history of snakes, but 47 year-old Najash (7), resembles the fossil opment, Cohn and Tickle (10) reported a many questions remain as to their origins, 48 marine snakes in having small hind legs marked expansion of the typical Hox ex- relationships, character evolution, and an- 49 without preserved digits but is more primi- pression domains, particularly those nor- cestral lifestyle. Resolution of these ques- 50 tive (1, 7). Tetrapodophis is also from South mally associated with the neck-trunk tions depends, ultimately, depends on the 51 America, and from a deposit that yields a boundary. They argued that the neck had recovery of further fossils and their thor- 52 mix of freshwater and terrestrial species, been lost in snakes and that this loss dis- ough and objective analysis. 53 but it is older (~113 million years old). Mar- rupted the molecular signals required for REFERENCES 54 till et al. (1) place it on the stem of the forelimb positioning and outgrowth. How- 1. D.M. Martill et al., Science XXX, xxx (2015). 55 snake evolutionary tree, below Najash and ever, in another snake, Pantherophis, the 2. M. C. Brandley et al., Evolution 62, 2042 (2008). 56 close to another early terrestrial snake, the Hox expression domains, although ex- 3. T. W. Reeder et al., PLOS ONE 10, e0118199 (2015). 4. M. W. Caldwell, Zool. J. Linn. Soc. 125, 115 (1999). 57 North American Coniophis, represented by panded and without sharp boundaries, re- 5. J. J. Head, Palaeontol. Electron. 18, 1 (2015). 58 vertebrae and attributed jaw elements. tain a regionalized pattern comparable to 6. E. Tchernov et al., Science 287, 2010 (2000). 59 Whereas fossils can yield information that of lizards with a distinct neck (9, 11). A 7. S. Apesteguía, H. Zaher, Nature 440, 1037 (2006). 8. C. Gomez et al., Nature 454, 335 (2008). on the sequence of anatomical changes in- parallel study of vertebral anatomy across a 9. J. M. Woltering et al., Dev. Biol. 332, 82 (2009). volved in any major transition, develop- wide range of snakes (12) revealed a similar 10. M. J. Cohn, C. Tickle, Nature 399, 474 (1999). sciencemag.org SCIENCE VOL. xxx • galley printed 6 July, 2015 • • For Issue Date: ???? 2 1 11. N. Di-Poï et al., Nature 464, 99 (2010). 12. J. J. Head, P. D. Polly, Nature 520, 86 (2015). 2 3 10.1126/science.aac5672 4 5 A four-limbed snake from the Cretaceous. 6 Tetrapodophis retains four limbs, each with five 7 digits, in an elongated body with 160 before-tail 8 vertebrae. 9 Credit: TKTKTKTKTK 10 11 Limbs or no limbs. (A) Martill et al. report the 12 discovery of a four-limbed snake, Tetrapodophis 13 amplectis, from the Cretaceous. (B) Schematic 14 showing independent development of the long 15 bodied, limb-reduced body plan amongst squa- 16 mates (not to scale). 17 18 Credit: panel A, D. M. Martill/University of 19 Portsmouth 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 sciencemag.org SCIENCE VOL. xxx • galley printed 6 July, 2015 • • For Issue Date: ???? 3 .